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ABA-mediated modulation of elevated CO2 on stomatal response to drought
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ScienceDirect ABA-mediated modulation of elevated CO2 on stomatal response to drought Shenglan Li1, Xiangnan Li3, Zhenhua Wei2 and Fulai Liu1,2 Elevated atmospheric CO2 concentration (e[CO2]) and soil water deficits have substantial effect on stomatal morphology and movement that regulate plant water relations and plant growth. e[CO2] could alleviate the impact of drought stress, thus contributing to crop yield. Xylem-borne abscisic acid (ABA) plays a crucial role in regulating stomatal aperture serving as first line of defence against drought; whereas e[CO2] may disrupt this fundamental drought adaptation mechanism by delaying the stomatal response to soil drying. We review the state-of-the-art knowledge on stomatal response to drought stress at e[CO2] and discuss the role of ABA in mediating these responses. Addresses 1 Department of Plant and Environmental Sciences, Faculty of Science, University of Copenhagen, Højbakkegaard Alle´ 13, DK-2630, Taastrup, Denmark 2 Key Laboratory of Agricultural Soil and Water Engineering in Arid and Semiarid Areas, Ministry of Education, Northwest A&F University, Yangling, Shaanxi 712100, China 3 Key Laboratory of Mollisols Agroecology, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Changchun 130102, China Corresponding authors: Li, Xiangnan ([email protected]), Liu, Fulai ([email protected])
Current Opinion in Plant Biology 2019,XX:xx–yy This review comes from a themed issue on AGRI Edited by David Edwards
https://doi.org/10.1016/j.pbi.2019.12.002 1369-5266/ã 2019 Elsevier Ltd. All rights reserved.
Introduction Since the Industrial Revolution the atmospheric carbon dioxide (CO2) concentration has been constantly increasing and is predicted to reach ca. 800 ppm at the end of this century [1]. The elevated CO2 concentration (e[CO2]) would stimulate global warming, causing declining freshwater resources in many agricultural regions around the world [2]. Global surface temperature very likely increases more than 2 C by year 2100 [3]. In addition, synthesis of four global climate datasets reveals a sharp increase of atmospheric vapour pressure deficit (VPD) as a consequence of global warming and declining in the www.sciencedirect.com
humidity of the atmosphere [4], which intensifies drought stress on plants. Stomata play a central role in controlling leaf gas exchange. Stomatal closing can be triggered by different environmental cues, including e[CO2], elevated leaf to air VPD (eVPD), soil water deficits, and abscisic acid (ABA) [5–8]. The positive fertilization effect of e[CO2] on crop yield might be offset by soil water deficits and eVPD, both induce desiccation of the leaf thus negatively affect crop yield [9,10]. However, the modulation of e[CO2] on plant drought response is complicated, wherein endogenous ABA may play an important role. In this review, we summarized works published in recent years that elucidated how does e[CO2] modulate the stomatal response to drought stress.
Stomatal response to drought under elevated CO2 To optimize water use efficiency (WUE) in varied environments, plants are capable of regulating their stomatal features including stomatal morphology (stomatal size, SS; stomatal density, SD) and stomatal movement (stomatal aperture, SA) to efficiently control the rates of water loss and CO2 intake [11]. Both e[CO2] and soil water deficits can reduce stomatal conductance (gs) [10], but the underlying mechanisms for inducing stomatal closure maybe different. It is widely accepted that soil dryinginduced stomatal closure is regulated by the root-to-shoot ABA signal at moderate soil water deficits and by the decrease in leaf turgor at severe drought [12]. The stomatal morphology can also be modified under prolonged drought [13,14]. Drought could lead to an increase in SD mainly caused by the decreased leaf expansion growth [15]. Drought also causes a reduction in SS and SA in wheat [16]. However, a study showed that SD increased under moderate drought and decreased under severe drought in Leymus chinensis [13]. SD often negatively correlated with SS and SA, rice plants with low SD might be able to maintain a low gs and survive severe drought; whilst an increased SA could compensate the negative effect of low SD under high temperature stress [17]. These studies suggest that the stomatal morphological features are plastic to abiotic stress. Similarly, e[CO2] also regulates gs. through a coordination of short-term response (change in SA) and long-term morphological adjustment (change in SD) [18,19,20,21]. e[CO2] could rapidly induce a decrease on SA, driven by the increase in the intercellular CO2 concentration [22]. For long-term response, plants with decreased SD have an improved Current Opinion in Plant Biology 2019, 13:1–7
Please cite this article in press as: Li S, et al.: ABA-mediated modulation of elevated CO2 on stomatal response to drought, Curr Opin Plant Biol (2020), https://doi.org/10.1016/j.pbi.2019.12.002
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WUE due to decreased transpiration use and unchanged photosynthesis [20,23]. The occurrence of different strategies of stomatal control in response to e[CO2] could be species specific [22]. It is believed that drought stress has a stronger impact on gs than e[CO2] [18,24]; whereas e[CO2] could attenuate the impact of drought stress on plant by enhanced WUE, attributing to the decreased gs and increased net photosynthetic rate (An) [24]. Further, it has been noticed that response of gs to drought was retarded in tomato plants grown under e[CO2] [25], which indicates that stomata become less sensitive to soil drying under e[CO2] (Figure 1). There is also evidence that e[CO2] might impair the effectiveness of stomatal closure, thus increasing the vulnerability of plants to severe water deficit and high temperatures [26]. Recent studies found a decrease of WUE in plants exposed to e[CO2] [27,28]. Moreover, increased leaf area under e[CO2] could ameliorate the adverse effect of drought stress [24], but it might exaggerate soil water deficits under prolonged drought, negatively affecting plant performance [29]. Nevertheless, the pros and cons of the effect of e[CO2]-modulated stomatal response on plant drought adaptation may coexist [24]. In addition, drought stress is often coupled with increases in ambient temperature [30], and recent study showed that e[CO2] enhanced heat tolerance in tomato by maintaining Figure 1
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A possible model for modulation of CO2 on gs response to progressive soil drying in tomato plant. The figure illustrates the sensitivity of gs to soil drying at ambient CO2 (a[CO2]) and elevated CO2 (e[CO2]) in tomato plant. gs indicates stomatal conductance. FTSW, the fraction of transpirable soil water, indicates the soil water content during drought stress period. When soil water is depleted to a FTSW threshold, gs starts to decrease in response to drought stress [25]. Plants grown under e[CO2] possess lower gs from onset of drought stress compared with those under a[CO2]. During progressive soil drying, plants have a lower FTSW threshold under e[CO2] (blue line) than the threshold under a[CO2] (red line), namely CO2 elevation retards gs response to drought stress and gs becomes less sensitive to drought under e[CO2]. Current Opinion in Plant Biology 2019, 13:1–7
water balance [19]. Thus, future research is necessary to focus on the multiple stress responses of plants grown under e[CO2].
ABA and stomatal regulation of drought-stressed plants under elevated CO2 Drought-induced stomatal closure is associated with increased ABA concentration derived from roots [12]. ABA is involved in different strategies of plants to avoid excessive water loss [31], and many reports demonstrated that stomatal responses to changes in atmospheric CO2 and VPD are associated with ABA levels in plants [32–34], though the underlying mechanisms remain largely elusive. Stomatal closure induced by e[CO2] and ABA are both triggered by the response in guard cell membrane channels and transporters, and ABA was involved in CO2sensing and signal transduction mechanisms [35]. Hus et al. [36] reported that basal ABA signaling was required to facilitate the stomatal response to e[CO2], and maintaining continuous low gs at e[CO2] also requires ABA. Chater et al. [35] further demonstrated that stomatal ABA response is in evolutionary terms ancestral to e[CO2] response. However, these reports are based on the short-term e[CO2]. For long-term e[CO2], the mechanism of stomatal response could be partly ABA-dependent [25]. Interestingly, e[CO2] might disrupt the ABAregulated stomatal control against drought [37]. Decreased gs was also found to be correlated with changes in plant hydraulics (leaf turgor pressure and plant hydraulic conductance) [38], indicating hydraulic signal maybe essential for stomatal control during drought under e[CO2]. Maintaining tissue hydration is of pivotal importance for plant survival under drought. This is achieved by finetuning regulation of leaf water relations, which is largely dependent on coordinated changes in gs and plant hydraulics [39]. When subjected to soil drying, plants change leaf hydraulic conductance (Kl) and root hydraulic conductance (Kr) in accordance with stomatal closure under different severities of drought stress [40] (Figure 2). Many studies showed that ABA could alter plant hydraulics under abiotic stress, including Kl and Kr [31,41,42] though the effect was inconsistent. Root ABA accumulation was reported to increase Kr in a dose-dependent manner [43], and ABA could stimulate root growth and root hydraulics under mild and moderate drought stress though the responses to severe drought were largely ABA independent [44]. Under severe drought stress, plant hydraulics might play major role in regulating stomatal responses [40]. Accordingly, the switch from ABA-limited to hydraulically limited stomatal aperture during drought stress may provide plants with a better water management strategy. Regulation of plant hydraulics by ABA under abiotic stress is associated with aquaporins (AQPs). AQPs play www.sciencedirect.com
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CO2 elevation modulates crop drought response Li et al.
Figure 2
Current Opinion in Plant Biology
Possible mechanism for stomatal control under different severity of drought stress. The figure shows models for different factors induced stomatal closure under moderate and severe drought respectively and how e[CO2] is involved in these mechanism. Dashed lines indicate controversial signaling. Under moderate drought stress, ABA is synthesized in response to drought [34] (1). ABA regulates activities of aquaporins (AQPs), which also called water channels that play an important role in regulating plant hydraulics [45]. Under moderate drought, ABA downregulates gene expression of APQs in leaves (2), thus decreasing leaf hydraulic conductance (Kl) (4). However, ABA has a controversial effect on root hydraulic conductance (Kr) (3). It may increase gene expression of AQPs in roots under moderate drought, thus increasing Kr (5) [45]. Changes in plant hydraulics induce stomatal closure (6). Under severe drought stress, plant hydraulics response are largely ABA independent [45]. Sharply decreased plant water potential (Cplant) [40] (8) may regulate gene expression of AQPs both in leaves and roots (9), thus decreasing plant hydraulics (10) and inducing stomatal closure (11). Meanwhile, e[CO2] decreases gene expression of AQPs in leaves and roots, and decrease Kl and Kr, thus inducing stomatal closure [49] (7, 12). In addition, e[CO2] is involved in other pathway regulating stomatal closure (Figure 3) (7).
an important role in transport of water and other small neutral molecules across cellular biological membrane [45]. Expression of plant AQPs could be regulated by drought stress and ABA [44], and Veselov et al. [46] reported that AQPs and ABA were both required to enhance Kr and maintain plant water potential under abiotic stress. Moreover, it is accepted that e[CO2] has great effect on plant hydraulics [47]. Along with the decreased gs, Kr was also decreased in response to e[CO2] [39,48]. Recent study reported that ABA-mediated regulation of plant hydraulics under e[CO2] was associated with AQPs [49]. These findings highlight a novel crosstalk between ABA and e[CO2] in regulating plant hydraulics, which merits further investigations.
Implications of elevated CO2-regulated drought adaptation mechanisms on crop growth and nutrient uptake
The modulation of e[CO2] on drought adaptation mechanisms of plants may have significant implication on crop www.sciencedirect.com
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performance under field conditions. Field crops could benefit from e[CO2] due to the increased An [50–52]. In cassava, e[CO2] increased carbon assimilation resulting in higher crop yield [53]. e[CO2] was also reported to influence crop quality [54,55]. Furthermore, it is generally accepted that the positive response of plants to e[CO2] is greater under abiotic stress conditions [53,54,56], and e[CO2] could enhance abiotic stress tolerance [51,57,58]. One of the strategies is to increase crop carbon (C) storage and promote remobilization of mineral nutrients, thus attenuating stress damage [10] (Figure 3). Studies have demonstrated that for C3 crops, e[CO2] has similar stimulation on biomass accumulation and yield under wellwatered and dry conditions. For C4 crops, however, stimulation by e[CO2] occurs only under dry conditions, indicating crops grown in areas with limited water availability could benefit from future e[CO2] environment [59]. In addition, it should be noted that plant drought adaptation mechanisms differ under intermediate and prolonged drought stress. Changes in rainfall distributions can lead to an increase in frequency and severity of droughts [60], and the delayed response of stomata to drought could be beneficial for crops exposing to intermediate drought but might be detrimental to crops suffering terminal drought. Free air CO2 enrichment (FACE) systems have been proven to be an efficient method to study crop yield response to climate changes under field conditions [52]. When combining the effect of CO2 and temperature, Wang et al. [61] reported that e[CO2] increased rice grain yield, but it could not compensate for the negative impacts of increased air temperature. Sun et al. [51] also found that e[CO2] greatly improved the fruit yield by increasing fruit number and fruit weight at low temperature, while decreased fruit yield at high temperature. Enhanced C uptake under e[CO2] could influence plant nitrogen (N) nutrition, resulting in metabolic changes that imposes a feedback on the C uptake [62–65] It is widely accepted that e[CO2] restrains N acquisition and N uptake, thus causing N limitation to crop production. However, Reich and Hobbie [66] documented that e[CO2] modulated N assimilation in a nitrate dosedependent manner. e[CO2] did not stimulate biomass production under ambient N condition, while under high N fertilization there was increased biomass production. The reduced N acquisition of plants grown at e[CO2] could be attributed to the decreased plant hydraulics and the downregulated expression of AQPs. A FACE study also showed a clear interaction of CO2 and N supply on biomass production [67]. When grown in open-top chambers, soybean represented a greater symbiotic N2 fixation under e[CO2] which was considered as a critical factor affecting N uptake [68]. In addition, plants grown under e[CO2] displayed enhanced production of nitric oxide (NO), which has a crucial role in protecting plants against various abiotic/biotic stresses [64], and NO is also Current Opinion in Plant Biology 2019, 13:1–7
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Figure 3
Decreased stomatal aperture
Increased carbon uptake
Decreased stomatal density Leaf enlargement
Decreased stomatal conductance
Decreased transpiration rate
DROUGHT
Root growth
Increased Plant growth
Increased WUE
Increased drought tolerance Current Opinion in Plant Biology
Possible mechanism for the modulation of e[CO2] on stomatal movements and plant growth. The figure shows a model that how CO2 elevation enhances drought tolerance due to stomatal and nutrient responses. For short-term response, e[CO2] decreases stomatal aperture [22]; For long-term response, e[CO2] decreases stomatal density (SD) [23]. Decreased SD and SA regulate leaf gas exchange, including decreased stomatal conductance (gs) and decreased transpiration rate (Tr) [24]. Accordingly, plant water use efficiency is enhanced, and plants can optimize water balance. Meanwhile, e[CO2] accelerates carbon (C) assimilation and uptake due to increased photosynthetic rate (An) [10]. Increased C uptake contributes to roots production and increases root to shoot ratio especially under drought stress [53]. Therefore, plant drought tolerance is enhanced under e[CO2].
reported to mediate e[CO2]-induced stomatal movements [69].
Conclusion and perspectives
The e[CO2], heat stress, eVPD and drought stress have multiple influences on stomatal response, plant water use and yield [5–8]. Plants control leaf gas exchange in response to environmental and endogenous signals to optimize WUE. Both e[CO2] and drought stress could regulate plant stomatal features [10], and e[CO2] delays stomatal response to drought [25] (Figure 1). However, recent studies showed that e[CO2] may have adverse effect on WUE and plant drought tolerance under prolonged drought stress due to impaired stomatal function [26]. In contrast, ABA and plant hydraulics also play a crucial role in regulating stomatal movements and plant water use [39]. Although mechanism of ABA-induced Current Opinion in Plant Biology 2019, 13:1–7
changes in plant hydraulics under drought stress has been explored [41], it still remains largely unknown about the significance of hydraulic and chemical signals in controlling stomatal aperture of drought-stressed plants. The prevailing consensus is that e[CO2] could attenuate drought damage via modulation of stomatal features and increase of C assimilation (Figure 3) [24,26,37]. Enhanced WUE under e[CO2] contributes to plant drought adaption [37], and increased C assimilation has a positive effect on root growth and crop yield [51,58]. Accordingly, plant drought tolerance is enhanced by e[CO2] (Figure 3). In contrast, e[CO2] along with an enhanced C uptake in plants influences the supply of N [62], but the restraint of N uptake is much dependent on the environmental factors and fertilization conditions [64,68]. In conclusion, there is a need to explore how e[CO2] modulates stomatal www.sciencedirect.com
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CO2 elevation modulates crop drought response Li et al.
response to multiple abiotic stress in different crop species, and what are the underlying bio-physiological mechanisms regulating stomatal movement and nutrient uptake of plants grown in a future warmer, drier and CO2enriched climate.
Conflict of interest statement Nothing declared.
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31. Parent B, Hachez C, Redondo E, Simonneau T, Chaumont F, Tardieu F: Drought and abscisic acid effects on aquaporin content translate into changes in hydraulic conductivity and leaf growth rate: a trans-scale approach. Plant Physiol 2009, 149:2000-2012. 32. Soar CJ, Speirs J, Maffei SM, Penrose AB, McCarthy MG, Loveys BR: Grape vine varieties Shiraz and Grenache differ in their stomatal response to VPD: apparent links with ABA physiology and gene expression in leaf tissue. Aust J Grape Wine Res 2006, 12:2-12. 33. Arve LE, Terfa MT, Gislerød HR, Olsen JE, Torre S: High relative air humidity and continuous light reduce stomata functionality by affecting the ABA regulation in rose leaves. Plant, Cell Environ 2013, 36:382-392. 34. Assmann SM, Jegla T: Guard cell sensory systems: recent insights on stomatal responses to light, abscisic acid, and CO2. Curr Opin Plant Biol 2016, 33:157-167. 35. Chater C, Peng K, Movahedi M, Dunn JA, Walker HJ, Liang YK, McLachlan DH, Casson S, Isner JC, Wilson I et al.: Elevated CO2-induced responses in stomata require ABA and ABA signaling. Curr Biol 2015, 25:2709-2716. 36. Hsu P, Takahashi Y, Munemasa S, Merilo E, Laanemets K, Waadt R, Pater D: Abscisic acid-independent stomatal CO2 signal transduction pathway and convergence of CO2 and ABA signaling downstream of OST1 Kinase. P Natl Acad Sci USA 2018, 115:9971-9980. This paper described a signal transduction model, in which rapid CO2 signal transduction leading to stomatal closure occurs via an ABAindependent pathway. Combined genetic, biochemical and whole-plant gas exchange analyses provided evidence that the convergent point of CO2 and ABA signaling was located downstream of OPEN STOMATA 1 (OST1/SnRK2.6), which was not in accordance with prevailing consensus. By using ABA biosynthesis mutant, this paper found CO2-induced stomatal closure was not mediated by ABA level, and CO2 elevation did not change ABA concentrations in guard cells. However, basal ABA signaling and OST1/SnRK2 activity were required to facilitate the stomatal response to e[CO2]. This further supported that ABA plays an important role in regulating stomatal response to e[CO2]. 37. Yan F, Li X, Liu F: ABA signaling and stomatal control in tomato plants exposure to progressive soil drying under ambient and elevated atmospheric CO2 concentration. Environ Exp Bot 2017, 139:99-104. 38. Miranda-apodaca J, Pe´rez-lo´pez U, Lacuesta M, Mena-petite A, Mun˜oz-rueda A: The interaction between drought and elevated CO2 in water relations in two grassland species is speciesspecific. J Plant Physiol 2018, 220:193-202. 39. Meinzer FC: Coordination of vapour and liquid phase water transport properties in plants. Environment 2002, 25:265-274. 40. Creek D, Blackman CJ, Brodribb TJ, Choat B, Tissue DT: Coordination between leaf, stem, and root hydraulics and gas exchange in three arid-zone angiosperms during severe drought and recovery. Plant Cell Environ 2018, 41:2869-2881. Current Opinion in Plant Biology 2019, 13:1–7
44. Kapilan R, Vaziri M, Zwiazek JJ: Regulation of aquaporins in plants under stress. Biol Res 2018, 51:4. 45. Reuscher S, Akiyama M, Mori C, Aoki K, Shibata D, Shiratake K: Genome-wide identification and expression analysis of aquaporins in tomato. PLoS One 2013, 8:e79052. 46. Veselov DS, Sharipova GV, Veselov SY, Dodd IC, Ivanov I, Kudoyarova GR: Rapid changes in root HvPIP2;2 aquaporins abundance and ABA concentration are required to enhance root hydraulic conductivity and maintain leaf water potential in response to increased evaporative demand. Funct Plant Biol 2018, 45:143-149. This paper offered evidence that sufficient ABA is necessary to adequately control root hydraulic conductivity (Lpr)in barley following a stepchange in VPD under air warming. By exposing ABA-deficient barley mutant and its parental wild type to high VPD resulted by air warming, the authors found that WT plants were capable of maintaining leaf water potential (Cl) due to increased Lpr enabling higher water flow from the roots, while mutant failed to maintain Cl during air warming due to lower Lpr, presenting an inability to respond to changes in air temperature. In addition, the correlation between root ABA content and Lpr was further supported by increased root hydraulic conductivity in both genotypes when treated with exogenous ABA. 47. Domec JC, Smith DD, McCulloh KA: A synthesis of the effects of atmospheric carbon dioxide enrichment on plant hydraulics: implications for whole-plant water use efficiency and resistance to drought. Plant Cell Environ 2017, 40:921-937. 48. Hao GY, Holbrook NM, Zwieniecki MA, Gutschick VP, BassiriRad H: Coordinated responses of plant hydraulic architecture with the reduction of stomatal conductance under elevated CO2 concentration. Tree Physiol 2018, 38:10411052. 49. Fang L, Abdelhakim LOA, Hegelund JN, Li S, Liu J, Peng X, Li X, Wei Z, Liu F: ABA-mediated regulation of leaf and root hydraulic conductance in tomato grown at elevated CO2 is associated with altered gene expression of aquaporins. Hortic Res 2019, 6:104. 50. Sakai H, Tokida T, Usui Y, Nakamura H: Yield responses to elevated CO2 concentration among Japanese rice cultivars released since 1882. Plant Prod Sci 2019, 22:352-366. 51. Sun P, Mantri N, Lou H, Hu Y, Sun D, Zhu Y, Dong T, Lu H: Effects of elevated CO2 and temperature on yield and fruit quality of strawberry (Fragaria ananassa Duch.) at two levels of nitrogen application. PLoS One 2012, 7. 52. Bunce J: Using FACE systems to screen wheat cultivars for yield increases at elevated CO2. Agronomy 2017, 7:8-13. 53. Cruz JL, Lecain DR, Alves AAC, Coelho MA, Coelho EF, Cruz JL, Lecain DR, Alves AAC, Antoˆnio M: Elevated CO2 reduces whole transpiration and substantially improves root production of cassava grown under water deficit. Arch Agron Soil Sci 2018, 64:1623-1634. 54. Kizildeniz T, Mekni I, Santesteban H, Pascual I, Morales F, Irigoyen JJ: Effects of climate change including elevated CO2 www.sciencedirect.com
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concentration, temperature and water deficit on growth, water status, and yield quality of grapevine (Vitis vinifera L.) cultivars. Agric Water Manag 2015, 159:155-164.
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55. Kizildeniz T, Pascual I, Irigoyen JJ, Morales F: Using fruit-bearing cuttings of grapevine and temperature gradient greenhouses to evaluate effects of climate change (elevated CO2 and temperature, and water deficit) on the cv. red and white Tempranillo. Yield and must quality in three consecutive growin. Agric Water Manag 2018, 202:299-310.
field conditions. By measuring leaf photosynthesis, nitrogen uptake, spikelet architecture and yield components over two rice growing seasons using a free-air CO2 enrichment facility, they found e[CO2] cannot compensate for the negative impacts of increased air temperature on rice yield, especially in the warmer season. However, the authors suggested that increasing biomass accumulation may improve the temperature tolerance of japonica rice and prevent yield reductions under future climate changes. Moreover, spikelet density was the factor that determined the rice yield, and the decreased number of spikelets per panicle was attributed to the N uptake.
56. Osborne T, Rose G, Wheeler T: Variation in the global-scale impacts of climate change on crop productivity due to climate model uncertainty and adaptation. Agric For Meteorol 2013, 170:183-194.
62. Vicca S, Phillips RP, Terrer C, Reich PB, Prentice IC, Stocker BD, Hungate BA, Finzi AC: Ecosystem responses to elevated CO2 governed by plant-soil interactions and the cost of nitrogen acquisition. New Phytol 2017, 217:507-522.
57. Ainsworth EA, Long SP: What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytol 2005, 165:351-372.
63. Lekshmy S, Jain V, Khetarpal S, Pandey R: Inhibition of nitrate uptake and assimilation in wheat seedlings grown under elevated CO2. Indian J Plant Physiol 2013, 18:23-29.
58. Uddin S, Lo¨w M, Parvin S, Fitzgerald GJ, Tausz-Posch S, Armstrong R, O’Leary G, Tausz M: Elevated [CO2] mitigates the effect of surface drought by stimulating root growth to access sub-soil water. PLoS One 2018, 13:1-20. This study investigated the effect of drought in shallow soil versus subsoil on agronomic and physiological responses of wheat to e[CO2] in a glasshouse experiment. The authors evaluated aboveground and belowground biomass, grain yield and yield components at three developmental stages (stem-elongation, anthesis and maturity). Their results showed that e[CO2] stimulated both aboveground and belowground biomass as well as grain yield; however, this stimulation was greater under well-watered than drought t, which was different from previous study. What interesting is that the greatest ‘CO2 fertilization effect’ was observed when drought was imposed in the top soil layer only, and this was associated with e[CO2]-stimulation of root growth. These results suggest that stimulation of belowground biomass under e[CO2] may help to mitigate the impact of surface drought on biomass and grain yield if sufficient water is available in the subsoil. 59. van der Kooi CJ, Reich M, Lo¨w M, De Kok LJ, Tausz M: Growth and yield stimulation under elevated CO2 and drought: a metaanalysis on crops. Environ Exp Bot 2016, 122:150-157. 60. de Oliveira MF, Marenco RA: Gas exchange, biomass allocation and water-use efficiency in response to elevated CO2 and drought in andiroba (Carapa surinamensis, Meliaceae). IForest 2019, 12:61-68. 61. Wang W, Cai C, Lam SK, Liu G, Zhu J: Elevated CO2 cannot compensate for japonica grain yield losses under increasing air temperature because of the decrease in spikelet density. Eur J Agron 2018, 99:21-29. In this paper, the authors combined different CO2 concentrations and different canopy air temperatures to evaluate whether e[CO2] compensated for the rice yield losses induced by increased air temperature under
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64. Adavi SB, Sathee L: Elevated CO2-induced production of nitric oxide differentially modulates nitrate assimilation and root growth of wheat seedlings in a nitrate dose-dependent manner. Protoplasma 2019, 256:147-159. 65. Loladze I: Hidden shift of the ionome of plants exposed to elevated CO2 depletes minerals at the base of human nutrition. eLife 2014, 2014:1-29. 66. Reich PB, Hobbie SE: Decade-long soil nitrogen constraint on the CO2 fertilization of plant biomass. Nat Clim Change 2013, 3:2-6. 67. Manderscheid R, Dier M, Erbs M, Sickora J, Weigel HJ: Nitrogen supply – A determinant in water use efficiency of winter wheat grown under free air CO2 enrichment. Agric Water Manag 2018, 210:70-77. This study investigated the effect of e[CO2] and nitrogen (N) fertilization on seasonal water use of crops using free air CO2 enrichment. Water use efficiency (WUE) was determined from the ratio of aboveground biomass production and evapotranspiration (ET). The authors found that increasing N supply enhanced biomass production, ET and WUE, and e[CO2] increased biomass by the same level among all N levels. However, there was a clear interaction of CO2 and N supply on ET and WUE. Simultaneously, the lower CO2 effect under N deficiency was reported to be from a smaller effect on ET. 68. Li Y, Yu Z, Liu X, Mathesius U, Wang G, Tang C, Wu J, Liu J, Zhang S, Jin J: Elevated CO2 increases nitrogen fixation at the reproductive phase contributing to various yield responses of soybean cultivars. Front Plant Sci 2017, 8. 69. Shi K, Li X, Zhang H, Zhang G, Liu Y, Zhou Y, Xia X, Chen Z, Yu J: Guard cell hydrogen peroxide and nitric oxide mediate elevated CO2-induced stomatal movement in tomato. New Phytol 2015, 208:342-353.
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ScienceDirect ABA-mediated modulation of elevated CO2 on stomatal response to drought Shenglan Li1, Xiangnan Li3, Zhenhua Wei2 and Fulai Liu1,2 Elevated atmospheric CO2 concentration (e[CO2]) and soil water deficits have substantial effect on stomatal morphology and movement that regulate plant water relations and plant growth. e[CO2] could alleviate the impact of drought stress, thus contributing to crop yield. Xylem-borne abscisic acid (ABA) plays a crucial role in regulating stomatal aperture serving as first line of defence against drought; whereas e[CO2] may disrupt this fundamental drought adaptation mechanism by delaying the stomatal response to soil drying. We review the state-of-the-art knowledge on stomatal response to drought stress at e[CO2] and discuss the role of ABA in mediating these responses. Addresses 1 Department of Plant and Environmental Sciences, Faculty of Science, University of Copenhagen, Højbakkegaard Alle´ 13, DK-2630, Taastrup, Denmark 2 Key Laboratory of Agricultural Soil and Water Engineering in Arid and Semiarid Areas, Ministry of Education, Northwest A&F University, Yangling, Shaanxi 712100, China 3 Key Laboratory of Mollisols Agroecology, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Changchun 130102, China Corresponding authors: Li, Xiangnan ([email protected]), Liu, Fulai ([email protected])
Current Opinion in Plant Biology 2019,XX:xx–yy This review comes from a themed issue on AGRI Edited by David Edwards
https://doi.org/10.1016/j.pbi.2019.12.002 1369-5266/ã 2019 Elsevier Ltd. All rights reserved.
Introduction Since the Industrial Revolution the atmospheric carbon dioxide (CO2) concentration has been constantly increasing and is predicted to reach ca. 800 ppm at the end of this century [1]. The elevated CO2 concentration (e[CO2]) would stimulate global warming, causing declining freshwater resources in many agricultural regions around the world [2]. Global surface temperature very likely increases more than 2 C by year 2100 [3]. In addition, synthesis of four global climate datasets reveals a sharp increase of atmospheric vapour pressure deficit (VPD) as a consequence of global warming and declining in the www.sciencedirect.com
humidity of the atmosphere [4], which intensifies drought stress on plants. Stomata play a central role in controlling leaf gas exchange. Stomatal closing can be triggered by different environmental cues, including e[CO2], elevated leaf to air VPD (eVPD), soil water deficits, and abscisic acid (ABA) [5–8]. The positive fertilization effect of e[CO2] on crop yield might be offset by soil water deficits and eVPD, both induce desiccation of the leaf thus negatively affect crop yield [9,10]. However, the modulation of e[CO2] on plant drought response is complicated, wherein endogenous ABA may play an important role. In this review, we summarized works published in recent years that elucidated how does e[CO2] modulate the stomatal response to drought stress.
Stomatal response to drought under elevated CO2 To optimize water use efficiency (WUE) in varied environments, plants are capable of regulating their stomatal features including stomatal morphology (stomatal size, SS; stomatal density, SD) and stomatal movement (stomatal aperture, SA) to efficiently control the rates of water loss and CO2 intake [11]. Both e[CO2] and soil water deficits can reduce stomatal conductance (gs) [10], but the underlying mechanisms for inducing stomatal closure maybe different. It is widely accepted that soil dryinginduced stomatal closure is regulated by the root-to-shoot ABA signal at moderate soil water deficits and by the decrease in leaf turgor at severe drought [12]. The stomatal morphology can also be modified under prolonged drought [13,14]. Drought could lead to an increase in SD mainly caused by the decreased leaf expansion growth [15]. Drought also causes a reduction in SS and SA in wheat [16]. However, a study showed that SD increased under moderate drought and decreased under severe drought in Leymus chinensis [13]. SD often negatively correlated with SS and SA, rice plants with low SD might be able to maintain a low gs and survive severe drought; whilst an increased SA could compensate the negative effect of low SD under high temperature stress [17]. These studies suggest that the stomatal morphological features are plastic to abiotic stress. Similarly, e[CO2] also regulates gs. through a coordination of short-term response (change in SA) and long-term morphological adjustment (change in SD) [18,19,20,21]. e[CO2] could rapidly induce a decrease on SA, driven by the increase in the intercellular CO2 concentration [22]. For long-term response, plants with decreased SD have an improved Current Opinion in Plant Biology 2019, 13:1–7
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WUE due to decreased transpiration use and unchanged photosynthesis [20,23]. The occurrence of different strategies of stomatal control in response to e[CO2] could be species specific [22]. It is believed that drought stress has a stronger impact on gs than e[CO2] [18,24]; whereas e[CO2] could attenuate the impact of drought stress on plant by enhanced WUE, attributing to the decreased gs and increased net photosynthetic rate (An) [24]. Further, it has been noticed that response of gs to drought was retarded in tomato plants grown under e[CO2] [25], which indicates that stomata become less sensitive to soil drying under e[CO2] (Figure 1). There is also evidence that e[CO2] might impair the effectiveness of stomatal closure, thus increasing the vulnerability of plants to severe water deficit and high temperatures [26]. Recent studies found a decrease of WUE in plants exposed to e[CO2] [27,28]. Moreover, increased leaf area under e[CO2] could ameliorate the adverse effect of drought stress [24], but it might exaggerate soil water deficits under prolonged drought, negatively affecting plant performance [29]. Nevertheless, the pros and cons of the effect of e[CO2]-modulated stomatal response on plant drought adaptation may coexist [24]. In addition, drought stress is often coupled with increases in ambient temperature [30], and recent study showed that e[CO2] enhanced heat tolerance in tomato by maintaining Figure 1
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A possible model for modulation of CO2 on gs response to progressive soil drying in tomato plant. The figure illustrates the sensitivity of gs to soil drying at ambient CO2 (a[CO2]) and elevated CO2 (e[CO2]) in tomato plant. gs indicates stomatal conductance. FTSW, the fraction of transpirable soil water, indicates the soil water content during drought stress period. When soil water is depleted to a FTSW threshold, gs starts to decrease in response to drought stress [25]. Plants grown under e[CO2] possess lower gs from onset of drought stress compared with those under a[CO2]. During progressive soil drying, plants have a lower FTSW threshold under e[CO2] (blue line) than the threshold under a[CO2] (red line), namely CO2 elevation retards gs response to drought stress and gs becomes less sensitive to drought under e[CO2]. Current Opinion in Plant Biology 2019, 13:1–7
water balance [19]. Thus, future research is necessary to focus on the multiple stress responses of plants grown under e[CO2].
ABA and stomatal regulation of drought-stressed plants under elevated CO2 Drought-induced stomatal closure is associated with increased ABA concentration derived from roots [12]. ABA is involved in different strategies of plants to avoid excessive water loss [31], and many reports demonstrated that stomatal responses to changes in atmospheric CO2 and VPD are associated with ABA levels in plants [32–34], though the underlying mechanisms remain largely elusive. Stomatal closure induced by e[CO2] and ABA are both triggered by the response in guard cell membrane channels and transporters, and ABA was involved in CO2sensing and signal transduction mechanisms [35]. Hus et al. [36] reported that basal ABA signaling was required to facilitate the stomatal response to e[CO2], and maintaining continuous low gs at e[CO2] also requires ABA. Chater et al. [35] further demonstrated that stomatal ABA response is in evolutionary terms ancestral to e[CO2] response. However, these reports are based on the short-term e[CO2]. For long-term e[CO2], the mechanism of stomatal response could be partly ABA-dependent [25]. Interestingly, e[CO2] might disrupt the ABAregulated stomatal control against drought [37]. Decreased gs was also found to be correlated with changes in plant hydraulics (leaf turgor pressure and plant hydraulic conductance) [38], indicating hydraulic signal maybe essential for stomatal control during drought under e[CO2]. Maintaining tissue hydration is of pivotal importance for plant survival under drought. This is achieved by finetuning regulation of leaf water relations, which is largely dependent on coordinated changes in gs and plant hydraulics [39]. When subjected to soil drying, plants change leaf hydraulic conductance (Kl) and root hydraulic conductance (Kr) in accordance with stomatal closure under different severities of drought stress [40] (Figure 2). Many studies showed that ABA could alter plant hydraulics under abiotic stress, including Kl and Kr [31,41,42] though the effect was inconsistent. Root ABA accumulation was reported to increase Kr in a dose-dependent manner [43], and ABA could stimulate root growth and root hydraulics under mild and moderate drought stress though the responses to severe drought were largely ABA independent [44]. Under severe drought stress, plant hydraulics might play major role in regulating stomatal responses [40]. Accordingly, the switch from ABA-limited to hydraulically limited stomatal aperture during drought stress may provide plants with a better water management strategy. Regulation of plant hydraulics by ABA under abiotic stress is associated with aquaporins (AQPs). AQPs play www.sciencedirect.com
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Figure 2
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Possible mechanism for stomatal control under different severity of drought stress. The figure shows models for different factors induced stomatal closure under moderate and severe drought respectively and how e[CO2] is involved in these mechanism. Dashed lines indicate controversial signaling. Under moderate drought stress, ABA is synthesized in response to drought [34] (1). ABA regulates activities of aquaporins (AQPs), which also called water channels that play an important role in regulating plant hydraulics [45]. Under moderate drought, ABA downregulates gene expression of APQs in leaves (2), thus decreasing leaf hydraulic conductance (Kl) (4). However, ABA has a controversial effect on root hydraulic conductance (Kr) (3). It may increase gene expression of AQPs in roots under moderate drought, thus increasing Kr (5) [45]. Changes in plant hydraulics induce stomatal closure (6). Under severe drought stress, plant hydraulics response are largely ABA independent [45]. Sharply decreased plant water potential (Cplant) [40] (8) may regulate gene expression of AQPs both in leaves and roots (9), thus decreasing plant hydraulics (10) and inducing stomatal closure (11). Meanwhile, e[CO2] decreases gene expression of AQPs in leaves and roots, and decrease Kl and Kr, thus inducing stomatal closure [49] (7, 12). In addition, e[CO2] is involved in other pathway regulating stomatal closure (Figure 3) (7).
an important role in transport of water and other small neutral molecules across cellular biological membrane [45]. Expression of plant AQPs could be regulated by drought stress and ABA [44], and Veselov et al. [46] reported that AQPs and ABA were both required to enhance Kr and maintain plant water potential under abiotic stress. Moreover, it is accepted that e[CO2] has great effect on plant hydraulics [47]. Along with the decreased gs, Kr was also decreased in response to e[CO2] [39,48]. Recent study reported that ABA-mediated regulation of plant hydraulics under e[CO2] was associated with AQPs [49]. These findings highlight a novel crosstalk between ABA and e[CO2] in regulating plant hydraulics, which merits further investigations.
Implications of elevated CO2-regulated drought adaptation mechanisms on crop growth and nutrient uptake
The modulation of e[CO2] on drought adaptation mechanisms of plants may have significant implication on crop www.sciencedirect.com
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performance under field conditions. Field crops could benefit from e[CO2] due to the increased An [50–52]. In cassava, e[CO2] increased carbon assimilation resulting in higher crop yield [53]. e[CO2] was also reported to influence crop quality [54,55]. Furthermore, it is generally accepted that the positive response of plants to e[CO2] is greater under abiotic stress conditions [53,54,56], and e[CO2] could enhance abiotic stress tolerance [51,57,58]. One of the strategies is to increase crop carbon (C) storage and promote remobilization of mineral nutrients, thus attenuating stress damage [10] (Figure 3). Studies have demonstrated that for C3 crops, e[CO2] has similar stimulation on biomass accumulation and yield under wellwatered and dry conditions. For C4 crops, however, stimulation by e[CO2] occurs only under dry conditions, indicating crops grown in areas with limited water availability could benefit from future e[CO2] environment [59]. In addition, it should be noted that plant drought adaptation mechanisms differ under intermediate and prolonged drought stress. Changes in rainfall distributions can lead to an increase in frequency and severity of droughts [60], and the delayed response of stomata to drought could be beneficial for crops exposing to intermediate drought but might be detrimental to crops suffering terminal drought. Free air CO2 enrichment (FACE) systems have been proven to be an efficient method to study crop yield response to climate changes under field conditions [52]. When combining the effect of CO2 and temperature, Wang et al. [61] reported that e[CO2] increased rice grain yield, but it could not compensate for the negative impacts of increased air temperature. Sun et al. [51] also found that e[CO2] greatly improved the fruit yield by increasing fruit number and fruit weight at low temperature, while decreased fruit yield at high temperature. Enhanced C uptake under e[CO2] could influence plant nitrogen (N) nutrition, resulting in metabolic changes that imposes a feedback on the C uptake [62–65] It is widely accepted that e[CO2] restrains N acquisition and N uptake, thus causing N limitation to crop production. However, Reich and Hobbie [66] documented that e[CO2] modulated N assimilation in a nitrate dosedependent manner. e[CO2] did not stimulate biomass production under ambient N condition, while under high N fertilization there was increased biomass production. The reduced N acquisition of plants grown at e[CO2] could be attributed to the decreased plant hydraulics and the downregulated expression of AQPs. A FACE study also showed a clear interaction of CO2 and N supply on biomass production [67]. When grown in open-top chambers, soybean represented a greater symbiotic N2 fixation under e[CO2] which was considered as a critical factor affecting N uptake [68]. In addition, plants grown under e[CO2] displayed enhanced production of nitric oxide (NO), which has a crucial role in protecting plants against various abiotic/biotic stresses [64], and NO is also Current Opinion in Plant Biology 2019, 13:1–7
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Figure 3
Decreased stomatal aperture
Increased carbon uptake
Decreased stomatal density Leaf enlargement
Decreased stomatal conductance
Decreased transpiration rate
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Increased Plant growth
Increased WUE
Increased drought tolerance Current Opinion in Plant Biology
Possible mechanism for the modulation of e[CO2] on stomatal movements and plant growth. The figure shows a model that how CO2 elevation enhances drought tolerance due to stomatal and nutrient responses. For short-term response, e[CO2] decreases stomatal aperture [22]; For long-term response, e[CO2] decreases stomatal density (SD) [23]. Decreased SD and SA regulate leaf gas exchange, including decreased stomatal conductance (gs) and decreased transpiration rate (Tr) [24]. Accordingly, plant water use efficiency is enhanced, and plants can optimize water balance. Meanwhile, e[CO2] accelerates carbon (C) assimilation and uptake due to increased photosynthetic rate (An) [10]. Increased C uptake contributes to roots production and increases root to shoot ratio especially under drought stress [53]. Therefore, plant drought tolerance is enhanced under e[CO2].
reported to mediate e[CO2]-induced stomatal movements [69].
Conclusion and perspectives
The e[CO2], heat stress, eVPD and drought stress have multiple influences on stomatal response, plant water use and yield [5–8]. Plants control leaf gas exchange in response to environmental and endogenous signals to optimize WUE. Both e[CO2] and drought stress could regulate plant stomatal features [10], and e[CO2] delays stomatal response to drought [25] (Figure 1). However, recent studies showed that e[CO2] may have adverse effect on WUE and plant drought tolerance under prolonged drought stress due to impaired stomatal function [26]. In contrast, ABA and plant hydraulics also play a crucial role in regulating stomatal movements and plant water use [39]. Although mechanism of ABA-induced Current Opinion in Plant Biology 2019, 13:1–7
changes in plant hydraulics under drought stress has been explored [41], it still remains largely unknown about the significance of hydraulic and chemical signals in controlling stomatal aperture of drought-stressed plants. The prevailing consensus is that e[CO2] could attenuate drought damage via modulation of stomatal features and increase of C assimilation (Figure 3) [24,26,37]. Enhanced WUE under e[CO2] contributes to plant drought adaption [37], and increased C assimilation has a positive effect on root growth and crop yield [51,58]. Accordingly, plant drought tolerance is enhanced by e[CO2] (Figure 3). In contrast, e[CO2] along with an enhanced C uptake in plants influences the supply of N [62], but the restraint of N uptake is much dependent on the environmental factors and fertilization conditions [64,68]. In conclusion, there is a need to explore how e[CO2] modulates stomatal www.sciencedirect.com
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response to multiple abiotic stress in different crop species, and what are the underlying bio-physiological mechanisms regulating stomatal movement and nutrient uptake of plants grown in a future warmer, drier and CO2enriched climate.
Conflict of interest statement Nothing declared.
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10. Paudel I, Halpern M, Wagner Y, Raveh E, Yermiyahu U, Hoch G, Klein T: Elevated CO2 compensates for drought effects in lemon saplings via stomatal downregulation, increased soil moisture, and increased wood carbon storage. Environ Exp Bot 2018, 148:117-127. 11. Mcadam SAM, Brodribb TJ: Stomatal innovation and the rise of seed plants. Ecol Lett 2012, 15:1-8. 12. Brodribb TJ, McAdam SAM: Abscisic acid mediates a divergence in the drought response of two conifers. Plant Physiol 2013, 162:1370-1377. 13. Xu Z, Zhou G: Responses of leaf stomatal density to water status and its relationship with photosynthesis in a grass. J Exp Bot 2008, 59:3317-3325. 14. Shabala L, Brodribb TJ, Zhou M, Shabala S: Understanding physiological and morphological traits contributing to drought tolerance in barley. J Agro Crop Sci 2019, 205:129-140. www.sciencedirect.com
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15. da Cunha Cruz Yasmini, Scarpa Ana Lı´via Martins, Pereira Marcio Paulo, de Castro Evaristo Mauro, Pereira Fabricio Jose´: Growth of typha domingensis as related to leaf physiological and anatomical modifications under drought conditions. Acta Physiol Plant 2019, 41:1-9. 16. Zhao W, Sun Y, Kjelgren R, Liu X: Response of stomatal density and bound gas exchange in leaves of maize to soil water deficit. Acta Physiol Plant 2015, 37:1704. 17. Caine RS, Yin X, Sloan J, Harrison EL, Mohammed U, Fulton T, Biswal AK, Dionora J, Chater CC, Coe RA et al.: Rice with reduced stomatal density conserves water and has improved drought tolerance under future climate conditions. New Phytol 2019, 221:371-384. In this paper, a rice cultivar with fewer stomata was created via manipulation of a development signal level. Low stomatal density rice plants along with low stomatal conductance were more capable of conserving water. When grown at elevated CO2, these plants were able to maintain their stomatal conductance and survive drought and high temperature (40 C) for longer compared with control plants. In addition, low stomatal density rice had equivalent or even improved yields. This work showed that rice plants with fewer stomata were more drought tolerant, providing a solution for plants to maintain yields and conserve water under warmer, high-CO2 world. 18. Xu Z, Jiang Y, Jia B, Zhou G: Elevated-CO2 response of stomata and its dependence on environmental factors. Front Plant Sci 2016, 7:1-15. 19. Zhang H, Pan C, Gu S, Ma Q, Zhang Y, Li X, Shi K: Stomatal movements are involved in elevated CO2-mitigated high temperature stress in tomato. Physiol Plant 2019, 165:569583. In this paper, a possible mechanism for how elevated atmospheric CO2 mitigated the negative effects of heat stress was described. e[CO2] could enhance heat tolerance due to maintain a balance between water retention and heat loss. This study showed that reduced stomatal aperture in response to e[CO2] could be explanation of enhanced heat tolerance. By silencing RESPIRATORY BURST OXIDASE 1 (RBOH1) which was associated with H2O2 accumulation, they found e[CO2]-induced stomatal closure and e[CO2]-enhanced water use efficiency were impeded as well as heat tolerance. 20. Habermann E, Dias de Oliveira EA, Contin DR, San Martin JAB, Curtarelli L, Gonzalez-Meler MA, Martinez CA: Stomatal development and conductance of a tropical forage legume are regulated by elevated [CO2] under moderate warming. Front Plant Sci 2019, 10:1-17. 21. Caldera HIU, De Costa WAJM, Woodward FI, Lake JA: Effects of elevated carbon dioxi de on stomatal characteristics and carbon isotope ratio of Arabidopsis thaliana ecotypes originating from an altitudinal gradient. Physiol Plant 2017, 159:74-92. 22. Haworth M, Killi D, Materassi A, Raschi A: Coordination of stomatal physiological behavior and morphology with carbon dioxide determines stomatal control. Am J Bot 2015, 102:677688. 23. Dunn Jessica, Hunt Lee, Afsharinafar Mana, Al Meselmani Moaed, Mitchell Alice, Howells Rhian, Wallington Emma, Fleming Andrew J, Gray Julie E: Reduced stomatal density in bread wheat leads to increased water-use efficiency. J Exp Bot 2019, 2013. 24. Temme AA, Liu JC, Cornwell WK, Aerts R, Cornelissen JHC: Hungry and thirsty: effects of CO2 and limited water availability on plant performance. Flora Morphol Distrib Funct Ecol Plants 2019, 254:188-193. 25. Liu J, Hu T, Fang L, Peng X, Liu F: CO2 elevation modulates the response of leaf gas exchange to progressive soil drying in tomato plants. Agric For Meteorol 2019, 268:181-188. This work established a new model of stomatal response of tomato plants to soil water deficits under e[CO2]. gs and transpiration rate (Tr) were decreased by e[CO2]. In addition, CO2 elevation retarded the response of leaf gas exchange to progressive soil drying in tomato plants, thus enhancing plant water use efficiency. However, delayed stomatal response also showed insensitivity of gs to drought stress under e [CO2]. In contrast, the mechanism by which decreases of gs in plants under a[CO2] could be regulated by endogenous ABA level, while under e [CO2] at moderate drought could be ABA-independent, although the responsiveness of gs to ABA was unaffected by CO2. Current Opinion in Plant Biology 2019, 13:1–7
Please cite this article in press as: Li S, et al.: ABA-mediated modulation of elevated CO2 on stomatal response to drought, Curr Opin Plant Biol (2020), https://doi.org/10.1016/j.pbi.2019.12.002
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26. Haworth M, Killi D, Materassi A, Raschi A, Centritto M: Impaired stomatal control is associated with reduced photosynthetic physiology in crop species grown at elevated [CO2]. Front Plant Sci 2016, 7:1-13. 27. Linares JC, Delgado-Huertas A, Camarero JJ, Merino J, Carreira JA: Competition and drought limit the response of water-use efficiency to rising atmospheric carbon dioxide in the Mediterranean fir Abies pinsapo. Oecologia 2009, 161:611624. 28. Becklin KM, Walker SM, Way DA, Ward JK: CO2 studies remain key to understanding a future world. New Phytol 2017, 214:3440.
41. Rosales MA, Maurel C, Nacry P: Abscisic acid coordinates dose-dependent developmental and hydraulic responses of roots to water deficit. Plant Physiol 2019, 180 pp.01546.2018. In this paper, different responses of root hydraulics under water deficits (WD) were described. The authors analyzed root system architecture and root hydraulic conductivity (Lpr) in hydroponically grown plants subjected to varying degrees of WD induced by various polyethylene glycol (PEG). Lpr was stimulated under mild WD conditions, while repressed under more severe conditions, showing a bell-shaped dependency on WD. Moreover, Lpr also showed a bell-shaped dependency on exogenous ABA, and their regulation by WD was attenuated when ABA biosynthesis was disturbed. Accordingly, they proposed that ABA acted as a coordinator and an integrator of root responses to mild and severe WD.
29. Manea A, Leishman MR: Competitive interactions between established grasses and woody plant seedlings under elevated CO2 levels are mediated by soil water availability. Oecologia 2015, 177:499-506.
42. Dayer S, Tyerman SD, Garnett T, Pagay V: Relationship between hydraulic and stomatal conductance and its regulation by root and leaf aquaporins under progressive water stress and recovery and exogenous application of ABA in Vitis vinifera L. ‘Syrah.’. Acta Hortic 2017, 1188:227-234.
30. Zandalinas SI, Mittler R, Balfago´n D, Arbona V, Go´mez-Cadenas A: Plant adaptations to the combination of drought and high temperatures. Physiol Plant 2018, 162:2-12.
43. Dodd IC: Abscisic acid and stomatal closure: a hydraulic conductance conundrum? New Phytol 2013, 197:6-8.
31. Parent B, Hachez C, Redondo E, Simonneau T, Chaumont F, Tardieu F: Drought and abscisic acid effects on aquaporin content translate into changes in hydraulic conductivity and leaf growth rate: a trans-scale approach. Plant Physiol 2009, 149:2000-2012. 32. Soar CJ, Speirs J, Maffei SM, Penrose AB, McCarthy MG, Loveys BR: Grape vine varieties Shiraz and Grenache differ in their stomatal response to VPD: apparent links with ABA physiology and gene expression in leaf tissue. Aust J Grape Wine Res 2006, 12:2-12. 33. Arve LE, Terfa MT, Gislerød HR, Olsen JE, Torre S: High relative air humidity and continuous light reduce stomata functionality by affecting the ABA regulation in rose leaves. Plant, Cell Environ 2013, 36:382-392. 34. Assmann SM, Jegla T: Guard cell sensory systems: recent insights on stomatal responses to light, abscisic acid, and CO2. Curr Opin Plant Biol 2016, 33:157-167. 35. Chater C, Peng K, Movahedi M, Dunn JA, Walker HJ, Liang YK, McLachlan DH, Casson S, Isner JC, Wilson I et al.: Elevated CO2-induced responses in stomata require ABA and ABA signaling. Curr Biol 2015, 25:2709-2716. 36. Hsu P, Takahashi Y, Munemasa S, Merilo E, Laanemets K, Waadt R, Pater D: Abscisic acid-independent stomatal CO2 signal transduction pathway and convergence of CO2 and ABA signaling downstream of OST1 Kinase. P Natl Acad Sci USA 2018, 115:9971-9980. This paper described a signal transduction model, in which rapid CO2 signal transduction leading to stomatal closure occurs via an ABAindependent pathway. Combined genetic, biochemical and whole-plant gas exchange analyses provided evidence that the convergent point of CO2 and ABA signaling was located downstream of OPEN STOMATA 1 (OST1/SnRK2.6), which was not in accordance with prevailing consensus. By using ABA biosynthesis mutant, this paper found CO2-induced stomatal closure was not mediated by ABA level, and CO2 elevation did not change ABA concentrations in guard cells. However, basal ABA signaling and OST1/SnRK2 activity were required to facilitate the stomatal response to e[CO2]. This further supported that ABA plays an important role in regulating stomatal response to e[CO2]. 37. Yan F, Li X, Liu F: ABA signaling and stomatal control in tomato plants exposure to progressive soil drying under ambient and elevated atmospheric CO2 concentration. Environ Exp Bot 2017, 139:99-104. 38. Miranda-apodaca J, Pe´rez-lo´pez U, Lacuesta M, Mena-petite A, Mun˜oz-rueda A: The interaction between drought and elevated CO2 in water relations in two grassland species is speciesspecific. J Plant Physiol 2018, 220:193-202. 39. Meinzer FC: Coordination of vapour and liquid phase water transport properties in plants. Environment 2002, 25:265-274. 40. Creek D, Blackman CJ, Brodribb TJ, Choat B, Tissue DT: Coordination between leaf, stem, and root hydraulics and gas exchange in three arid-zone angiosperms during severe drought and recovery. Plant Cell Environ 2018, 41:2869-2881. Current Opinion in Plant Biology 2019, 13:1–7
44. Kapilan R, Vaziri M, Zwiazek JJ: Regulation of aquaporins in plants under stress. Biol Res 2018, 51:4. 45. Reuscher S, Akiyama M, Mori C, Aoki K, Shibata D, Shiratake K: Genome-wide identification and expression analysis of aquaporins in tomato. PLoS One 2013, 8:e79052. 46. Veselov DS, Sharipova GV, Veselov SY, Dodd IC, Ivanov I, Kudoyarova GR: Rapid changes in root HvPIP2;2 aquaporins abundance and ABA concentration are required to enhance root hydraulic conductivity and maintain leaf water potential in response to increased evaporative demand. Funct Plant Biol 2018, 45:143-149. This paper offered evidence that sufficient ABA is necessary to adequately control root hydraulic conductivity (Lpr)in barley following a stepchange in VPD under air warming. By exposing ABA-deficient barley mutant and its parental wild type to high VPD resulted by air warming, the authors found that WT plants were capable of maintaining leaf water potential (Cl) due to increased Lpr enabling higher water flow from the roots, while mutant failed to maintain Cl during air warming due to lower Lpr, presenting an inability to respond to changes in air temperature. In addition, the correlation between root ABA content and Lpr was further supported by increased root hydraulic conductivity in both genotypes when treated with exogenous ABA. 47. Domec JC, Smith DD, McCulloh KA: A synthesis of the effects of atmospheric carbon dioxide enrichment on plant hydraulics: implications for whole-plant water use efficiency and resistance to drought. Plant Cell Environ 2017, 40:921-937. 48. Hao GY, Holbrook NM, Zwieniecki MA, Gutschick VP, BassiriRad H: Coordinated responses of plant hydraulic architecture with the reduction of stomatal conductance under elevated CO2 concentration. Tree Physiol 2018, 38:10411052. 49. Fang L, Abdelhakim LOA, Hegelund JN, Li S, Liu J, Peng X, Li X, Wei Z, Liu F: ABA-mediated regulation of leaf and root hydraulic conductance in tomato grown at elevated CO2 is associated with altered gene expression of aquaporins. Hortic Res 2019, 6:104. 50. Sakai H, Tokida T, Usui Y, Nakamura H: Yield responses to elevated CO2 concentration among Japanese rice cultivars released since 1882. Plant Prod Sci 2019, 22:352-366. 51. Sun P, Mantri N, Lou H, Hu Y, Sun D, Zhu Y, Dong T, Lu H: Effects of elevated CO2 and temperature on yield and fruit quality of strawberry (Fragaria ananassa Duch.) at two levels of nitrogen application. PLoS One 2012, 7. 52. Bunce J: Using FACE systems to screen wheat cultivars for yield increases at elevated CO2. Agronomy 2017, 7:8-13. 53. Cruz JL, Lecain DR, Alves AAC, Coelho MA, Coelho EF, Cruz JL, Lecain DR, Alves AAC, Antoˆnio M: Elevated CO2 reduces whole transpiration and substantially improves root production of cassava grown under water deficit. Arch Agron Soil Sci 2018, 64:1623-1634. 54. Kizildeniz T, Mekni I, Santesteban H, Pascual I, Morales F, Irigoyen JJ: Effects of climate change including elevated CO2 www.sciencedirect.com
Please cite this article in press as: Li S, et al.: ABA-mediated modulation of elevated CO2 on stomatal response to drought, Curr Opin Plant Biol (2020), https://doi.org/10.1016/j.pbi.2019.12.002
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concentration, temperature and water deficit on growth, water status, and yield quality of grapevine (Vitis vinifera L.) cultivars. Agric Water Manag 2015, 159:155-164.
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55. Kizildeniz T, Pascual I, Irigoyen JJ, Morales F: Using fruit-bearing cuttings of grapevine and temperature gradient greenhouses to evaluate effects of climate change (elevated CO2 and temperature, and water deficit) on the cv. red and white Tempranillo. Yield and must quality in three consecutive growin. Agric Water Manag 2018, 202:299-310.
field conditions. By measuring leaf photosynthesis, nitrogen uptake, spikelet architecture and yield components over two rice growing seasons using a free-air CO2 enrichment facility, they found e[CO2] cannot compensate for the negative impacts of increased air temperature on rice yield, especially in the warmer season. However, the authors suggested that increasing biomass accumulation may improve the temperature tolerance of japonica rice and prevent yield reductions under future climate changes. Moreover, spikelet density was the factor that determined the rice yield, and the decreased number of spikelets per panicle was attributed to the N uptake.
56. Osborne T, Rose G, Wheeler T: Variation in the global-scale impacts of climate change on crop productivity due to climate model uncertainty and adaptation. Agric For Meteorol 2013, 170:183-194.
62. Vicca S, Phillips RP, Terrer C, Reich PB, Prentice IC, Stocker BD, Hungate BA, Finzi AC: Ecosystem responses to elevated CO2 governed by plant-soil interactions and the cost of nitrogen acquisition. New Phytol 2017, 217:507-522.
57. Ainsworth EA, Long SP: What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytol 2005, 165:351-372.
63. Lekshmy S, Jain V, Khetarpal S, Pandey R: Inhibition of nitrate uptake and assimilation in wheat seedlings grown under elevated CO2. Indian J Plant Physiol 2013, 18:23-29.
58. Uddin S, Lo¨w M, Parvin S, Fitzgerald GJ, Tausz-Posch S, Armstrong R, O’Leary G, Tausz M: Elevated [CO2] mitigates the effect of surface drought by stimulating root growth to access sub-soil water. PLoS One 2018, 13:1-20. This study investigated the effect of drought in shallow soil versus subsoil on agronomic and physiological responses of wheat to e[CO2] in a glasshouse experiment. The authors evaluated aboveground and belowground biomass, grain yield and yield components at three developmental stages (stem-elongation, anthesis and maturity). Their results showed that e[CO2] stimulated both aboveground and belowground biomass as well as grain yield; however, this stimulation was greater under well-watered than drought t, which was different from previous study. What interesting is that the greatest ‘CO2 fertilization effect’ was observed when drought was imposed in the top soil layer only, and this was associated with e[CO2]-stimulation of root growth. These results suggest that stimulation of belowground biomass under e[CO2] may help to mitigate the impact of surface drought on biomass and grain yield if sufficient water is available in the subsoil. 59. van der Kooi CJ, Reich M, Lo¨w M, De Kok LJ, Tausz M: Growth and yield stimulation under elevated CO2 and drought: a metaanalysis on crops. Environ Exp Bot 2016, 122:150-157. 60. de Oliveira MF, Marenco RA: Gas exchange, biomass allocation and water-use efficiency in response to elevated CO2 and drought in andiroba (Carapa surinamensis, Meliaceae). IForest 2019, 12:61-68. 61. Wang W, Cai C, Lam SK, Liu G, Zhu J: Elevated CO2 cannot compensate for japonica grain yield losses under increasing air temperature because of the decrease in spikelet density. Eur J Agron 2018, 99:21-29. In this paper, the authors combined different CO2 concentrations and different canopy air temperatures to evaluate whether e[CO2] compensated for the rice yield losses induced by increased air temperature under
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64. Adavi SB, Sathee L: Elevated CO2-induced production of nitric oxide differentially modulates nitrate assimilation and root growth of wheat seedlings in a nitrate dose-dependent manner. Protoplasma 2019, 256:147-159. 65. Loladze I: Hidden shift of the ionome of plants exposed to elevated CO2 depletes minerals at the base of human nutrition. eLife 2014, 2014:1-29. 66. Reich PB, Hobbie SE: Decade-long soil nitrogen constraint on the CO2 fertilization of plant biomass. Nat Clim Change 2013, 3:2-6. 67. Manderscheid R, Dier M, Erbs M, Sickora J, Weigel HJ: Nitrogen supply – A determinant in water use efficiency of winter wheat grown under free air CO2 enrichment. Agric Water Manag 2018, 210:70-77. This study investigated the effect of e[CO2] and nitrogen (N) fertilization on seasonal water use of crops using free air CO2 enrichment. Water use efficiency (WUE) was determined from the ratio of aboveground biomass production and evapotranspiration (ET). The authors found that increasing N supply enhanced biomass production, ET and WUE, and e[CO2] increased biomass by the same level among all N levels. However, there was a clear interaction of CO2 and N supply on ET and WUE. Simultaneously, the lower CO2 effect under N deficiency was reported to be from a smaller effect on ET. 68. Li Y, Yu Z, Liu X, Mathesius U, Wang G, Tang C, Wu J, Liu J, Zhang S, Jin J: Elevated CO2 increases nitrogen fixation at the reproductive phase contributing to various yield responses of soybean cultivars. Front Plant Sci 2017, 8. 69. Shi K, Li X, Zhang H, Zhang G, Liu Y, Zhou Y, Xia X, Chen Z, Yu J: Guard cell hydrogen peroxide and nitric oxide mediate elevated CO2-induced stomatal movement in tomato. New Phytol 2015, 208:342-353.
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